Environ Sci Pollut Res DOI 10.1007/s11356-014-3180-5 WORLDWIDE INTEGRATED ASSESSMENT OF THE IMPACT OF SYSTEMIC PESTICIDES ON BIODIVERSITY AND ECOSYSTEMS A review of the direct and indirect effects of neonicotinoids and fipronil on vertebrate wildlife David Gibbons & Christy Morrissey & Pierre Mineau Received: 7 April 2014 /Accepted: 6 June 2014 # The Author(s) 2014. This article is published with open access at Springerlink.com Abstract Concerns over the role of pesticides affecting ver- at levels below those which will cause mortality to freshwater tebrate wildlife populations have recently focussed on system- vertebrates, although sub-lethal effects may occur. Some re- ic products which exert broad-spectrum toxicity. Given that corded environmental concentrations of fipronil, however, the neonicotinoids have become the fastest-growing class of may be sufficiently high to harm fish. Indirect effects are insecticides globally, we review here 150 studies of their direct rarely considered in risk assessment processes and there is a (toxic) and indirect (e.g. food chain) effects on vertebrate paucity of data, despite the potential to exert population-level wildlife—mammals, birds, fish, amphibians and reptiles. We effects. Our research revealed two field case studies of indirect focus on two neonicotinoids, imidacloprid and clothianidin, effects. In one, reductions in invertebrate prey from both and a third insecticide, fipronil, which also acts in the same imidacloprid and fipronil uses led to impaired growth in a fish systemic manner. Imidacloprid and fipronil were found to be species, and in another, reductions in populations in two lizard toxic to many birds and most fish, respectively. All three species were linked to effects of fipronil on termite prey. insecticides exert sub-lethal effects, ranging from genotoxic Evidence presented here suggests that the systemic insecti- and cytotoxic effects, and impaired immune function, to re- cides, neonicotinoids and fipronil, are capable of exerting duced growth and reproductive success, often at concentra- direct and indirect effects on terrestrial and aquatic vertebrate tions well below those associated with mortality. Use of wildlife, thus warranting further review of their environmental imidacloprid and clothianidin as seed treatments on some safety. crops poses risks to small birds, and ingestion of even a few treated seeds could cause mortality or reproductive impair- Keywords Pesticide . Neonicotinoid . Imidacloprid . ment to sensitive bird species. In contrast, environmental Clothianidin . Fipronil . Vertebrate . Wildlife . Mammals . concentrations of imidacloprid and clothianidin appear to be Birds . Fish . Amphibians . Reptiles . Risk assessment Responsible editor: Philippe Garrigues D. Gibbons (*) Overview of impacts of pesticides on vertebrate wildlife RSPB Centre for Conservation Science, RSPB, The Lodge, Sandy, Bedfordshire SG19 2DL, UK Although vertebrates are the intended target of only 2 % of e-mail: [email protected] pesticides on the market, the unintentional impacts of pesti- C. Morrissey cides on vertebrate populations have been marked and are Department of Biology, University of Saskatchewan, 112 Science well documented (e.g. Sánchez-Bayo 2011). Pesticides can Place, Saskatoon, Saskatchewan S7N 5E2, Canada exert their impact on vertebrates either directly, through their toxicity, or indirectly, for example, by reducing their food C. Morrissey School of Environment and Sustainability, University of supply. Saskatchewan, 117 Science Place, Saskatoon, Saskatchewan S7N Direct effects may be the result of several different expo- 5E2, Canada sure pathways: through ingestion of the formulated product (e.g. birds eating seeds coated with insecticide; Avery et al. P. Mineau Pierre Mineau Consulting, 124 Creekside Drive, Salt Spring 1997; Prosser and Hart 2005), through uptake via the skin Island V8K 2E4, Canada following a spray event (Mineau 2011) or by eating Environ Sci Pollut Res contaminated prey. Probably the most notable example among acetylcholine receptors (nAChR) in the postsynaptic neuron, the latter exposure pathway was the dramatic impact that acting as ‘false neurotransmitters’ (agonists). This interference organochlorine pesticides, especially DDT and its metabolite with acetylcholine neurotransmitter signalling causes contin- DDE, had on populations of birds of prey (Ratcliffe 1967; uous activation of the receptor, leading to symptoms of neu- Newton 1995). Depending on the extent of intoxication, direct rotoxicity. Neonicotinoids have greater affinity for, and thus effects of pesticides can either kill vertebrates outright or exert bind more strongly to, insect than mammalian or other verte- sub-lethal effects, for example, on growth and reproduction brate receptors, so their toxicity to mammals is lower than it is (Sánchez-Bayo 2011). Progress since the organo-chlorine era to insects and the reversibility of intoxication higher has helped ensure that compounds that are currently being (Tomizawa and Casida 2005; Jeschke et al. 2011). Fipronil developed and registered are generally less persistent and do works similarly, but instead binds to the gamma-aminobutyric not as readily bio-accumulate in food webs. acid (GABA) receptors, resulting in similar continuous central More recently, however, interest has turned to investigating nervous system activity (Tingle et al. 2000, 2003). As with the potential for indirect effects which are typically mediated neonicotinoids, fipronil has a lower affinity to vertebrate than through loss in quantity or quality of prey associated with to invertebrate receptors (Grant et al. 1998). Despite the lower pesticide use, or through habitat modification (Sotherton and toxicity of these products to vertebrates than to invertebrates, Holland 2002; Boatman et al. 2004;Morrisetal.2005). This there is still ample evidence that vertebrates show toxic ef- is especially the case in jurisdictions where the use of highly fects, albeit at markedly higher concentrations than for many toxic pesticides has been controlled and the frequency of target and non-target invertebrate species (e.g. Tingle et al. direct impacts reduced (Mineau et al. 1999). 2000, 2003; Cox 2001; SERA 2005; DeCant and Barrett Over the last 2 decades, a new class of insecticides, the 2010; Mineau and Palmer 2013). neonicotinoids, has become the most important and fastest growing of the five major chemical classes of insecticides on the global market (Jeschke and Nauen 2008; Jeschke et al. Materials and methods 2011; Tomizawa and Casida 2011;CasidaandDurkin2013). When used as plant protection products, neonicotinoids act by To assess the likely impacts of neonicotinoids and fipronil on becoming distributed systemically throughout the growing vertebrates, a literature search was undertaken using Web of plant following seed or soil applications. Another recent in- Science and Google Scholar. Search terms were [product] and secticide, fipronil, a phenyl-pyrazole (fiprole) rather than a [taxon], where [product] was either neonicotinoid, neonicotinoid, also acts in the same manner and has a similar imidacloprid, thiacloprid, clothianidin, thiamethoxam, toxicity and persistence profile (Grant et al. 1998). Conse- acetamiprid, nitenpyram, dinotefuran or fipronil; and [taxon] quently, the neonicotinoids and fipronil are sometimes jointly was either vertebrate*, mammal*, bird*, reptile*, amphibian* termed ‘systemic insecticides’, although there are also older and fish*. In addition, specific searches were made on a few products which could be termed ‘systemic’, for example, the common toxicity test species (e.g. rat) and by following up organo-phosphorous insecticide acephate and the organo- references cited in the publications found by the search. The arsenical, monosodium methanearsonate. Neonicotinoids review also draws heavily on the recently published report by are, in particular, commonly applied as seed treatments. The Mineau and Palmer (2013) on the direct and indirect toxicity use of seed treatments as a convenient and effective applica- of neonicotinoids to birds. Several industry studies, which tion method has widespread appeal in the farming industry. have not been formally published but which were part of Consequently, systemic seed treatments are now used on the product approval processes, were reviewed by Mineau and majority of agricultural crops worldwide (Garthwaite et al. Palmer and have been included here. While industry studies 2003; Jeschke et al. 2011). have been reviewed by regulators and may receive as much Here, we build on the reviews of others (e.g. Goulson 2013; critical review as in the open peer-reviewed literature, empha- Köhler and Triebskorn 2013; Mineau and Palmer 2013)to sis here is on published reports and the primary literature. examine the evidence and potential for direct and indirect The following information was extracted from each study: effects of two common systemic neonicotinoid insecticides, the product used, its dose and whether or not it was presented imidacloprid and clothianidin, along with fipronil on verte- as a single dose (acute) or over a period of time (chronic; e.g. brate wildlife. over 30 days); the effects on individual organisms, specifically whether there was an impact on survival, reproduction, growth and development, or other sub-lethal effects, such as Mode of action of the systemic insecticides neurobehavioural, genotoxic, cytotoxic, and immunotoxic; the impact on populations of the animal (e.g.